Non-Genetic Inheritance in Evolution

It’s no secret that the Modern Synthesis is not quite so modern anymore, and is due for an overhaul soon enough, with the addition of several components in an Extended Evolutionary Synthesis. One of these additions will probably be non-genetic inheritance (Danchin et al., 2011).

Non-genetic inheritance gets a lot of flak, from me included. Criticisms are handily summarised in Dickins & Rahman (2012). This post marks my stance starting to change on the whole concept after some random thinking and reading about it.

First off, it must be made clear that there is a lot of confusion about the concept that leads to invalid criticisms. The most common of these is the conflation of it with soft inheritance, a debunked early 20th century concept (Bonduriansky, 2012). Soft inheritance involves direct changes to DNA, while non-genetic inheritance does not. I don’t know how to confusion came about.

Non-genetic inheritance is also not mere phenotypic plasticity or behavioural plasticity, although they certainly are related (Bonduriansky & Day, 2009). Plasticities are the result of environmental variability causing epigenetic or behavioural changes. It was thinking about phenotypic plasticity that triggered my change in opinion.

I remember clearly, at the end of one of my public natural selection lectures, an audience member asked about what the role of epigenetics is in evolution. I mumbled something about epigenetics evolving as a genetic mechanism to allow plasticity in the face of ever-changing environments, since generational times exceed the rate of change in environments, making regular genetic fixation and adaptation an impossible response to changing environments. In other words, I chained epigenetics directly to genetics, causing a logical loop where epigenetics cannot be untied from genetic inheritance.

But the research is stacking up against this traditional view that I parroted. Not all plasticities qualify for non-genetic inheritance. Non-genetic inheritance is the transmission of such epigenetic states and of learned mechanisms to successive generations, without classical heredity.

We know that these can occur. “Culture”, broadly defined as the transmission of non-learned behaviours across generations, is the result of non-genetic inheritance (Galef & Laland, 2005). On more certain terms, epigenetic inheritance, while disputed for a long time, has now been shown in most organisms (Jablonka, 2012).

What this means is that there must be a decoupling between classical genetic inheritance and non-genetic inheritance. Of course, this decoupling is not complete, they will affect each other, especially when we consider evolutionary timescales. As a trivial example, consider the spread of lactose tolerance among humans. It’s a genetic change that got fixated not only by classical population genetics mechanisms, but also by the non-genetic inheritance of farming culture (Laland et al., 2010). The study of gene-culture coevolution is littered with similar examples demonstrating the need to look beyond just genetics in order to get an integrated view of how evolution proceeds. This realisation is also bleeding into theory, and is leading to interesting results (Geoghegan & Spencer, 2012) and even framework models that completely integrate non-genetic inheritance with established population genetics (Day & Bonduriansky, 2011).

Evolutionary biology quite often progresses by stubborn debate, especially when it comes to proposals of new foundational mechanisms. This is no different. You have a load of indifference from most, and two polarised camps with researchers entrenched in their positions: the staunch traditionalists who try to explain everything with the Modern Synthesis (Dickins & Rahman, 2012), and those who will maybe exaggerate the role of non-genetic inheritance (Jablonka & Lamb, 2006). The debate centers around the relative importance in the grand scheme of evolution. Is it really universal, does it occur only in unique cases, is it an active sidekick to natural selection et al. but not too noticeable, is it a mere statistical illusion and not even present? Future research, which will hopefully be dominated by empirical rather than theoretical work (so that the group selection debacle doesn’t happen again), should make it all clear. But only after several years (decades?) of highly entertaining mudfights. Good times lie ahead for those of us who care about this topic and are on the fence.

References:

Bonduriansky R. 2012. Rethinking heredity, again. TrEE 27, 330-336.

Bonduriansky R & Day R. 2009. Nongenetic Inheritance and Its Evolutionary Implications. Annual Review of Ecology, Evolution, and Systematics 40, 103-125.

Danchin É, Charmantier A, Champagne FA, Mesoudi A, Pujol B & Blanchet S. 2011. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nature Reviews Genetics 12, 475-486.

Day R & Bonduriansky R. 2011. A Unified Approach to the Evolutionary Consequences of Genetic and Nongenetic Inheritance. The American Naturalist 178, E18-E36.

Dickins TE & Rahman Q. 2012. The extended evolutionary synthesis and the role of soft inheritance in evolution. Proc. R. Soc. B 279, 2913-2921.

Galef Jr. BG & Laland KN. 2005. Social Learning in Animals: Empirical Studies and Theoretical Models. BioScience 55, 489-499.

Geoghegan JL & Spencer HG. 2012. Population-epigenetic models of selection. Theoretical Population Biology 81, 232-242.

Jablonka E. 2012. Epigenetic inheritance and plasticity: The responsive germline. Progress in Biophysics and Molecular Biology 111, 99-107.

Jablonka E & Lamb MJ. 2006. Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life.

Laland KN, Odling-Smee J & Myles S. 2010. How culture shaped the human genome: bringing genetics and the human sciences together. Nature Reviews Genetics 11, 137-148.

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